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Diversity and distribution of cephalopod species off the coast of Chile Christian M. Ibáñez a; Patricio A. Camus bc; Francisco J. Rocha d a Instituto de Ecología y Biodiversidad, Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile b Departamento de Ecología Costera, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Concepción, Chile c Center for Advanced Studies in Ecology and Biodiversity, d Departamento de Ecología y Biología Animal, Universidad de Vigo, Vigo, España

Online Publication Date: 01 July 2009

To cite this Article Ibáñez, Christian M., Camus, Patricio A. and Rocha, Francisco J.(2009)'Diversity and distribution of cephalopod species off the coast of Chile',Marine Biology Research,5:4,374 — 384 To link to this Article: DOI: 10.1080/17451000802534873 URL: http://dx.doi.org/10.1080/17451000802534873

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ORIGINAL ARTICLE

Diversity and distribution of cephalopod species off the coast of Chile

CHRISTIAN M. IBA´ N˜ EZ1*, PATRICIO A. CAMUS2,3 & FRANCISCO J. ROCHA4

1Instituto de Ecologıá y Biodiversidad, Departamento de Ciencias Ecolo´gicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile; 2Departamento de Ecologıá Costera, Facultad de Ciencias, Universidad Cato´lica de la Santı´sima Concepcioń, Concepcioń, Chile; 3Center for Advanced Studies in Ecology and Biodiversity; 4Departamento de Ecologıá y Biologıá Animal, Universidad de Vigo, Vigo, Espanã

Abstract Cephalopods are increasingly acknowledged as an ecologically important group in Chilean ecosystems, but are also one of their less-known biogeographic components. Notably, this group is represented virtually exclusively by non-endemic species, although we hypothesized that their distribution over the coast should be constrained by similar physical determinants to those affecting endemic taxa. We thus present a first evaluation of the latitudinal patterns of diversity and distribution of cephalopod species in Chile, based on geographical data obtained from a review of the available literature. We constructed presenceÁabsence binary matrices of coastal and oceanic species in 20 latitudinal units (28), for then calculating the respective similarity matrices to obtain a distribution dendrogram using hierarchical cluster analysis (UPGM). The original binary matrices were resampled performing 1000 stochastic reassignments to calculating the 95th percentile as the criterion to identify significant clusters. Statistical comparisons between distributional groupings were performed using ANOSIM. We recorded 86 cephalopods in Chile, including oceanic (71) and coastal (15) species. Species richness showed two major breaks at 308 S and 428 S, and decreased toward higher latitudes. Cephalopod species showed well-defined endpoints of distribution within the Chilean coast, differentiating three main biogeographical units: northern (18Á308 S), central (30Á428 S) and southern (42Á568 S) areas. Biogeographical patterns of cephalopod species in Chile showed no particular difference with those already described for most Chilean taxa. The marked distribution breaks of cephalopods at 308 and 428 S suggest that external forcing and physical factors other than temperature gradients may strongly constrain their dispersal.

Key words: Biogeography, Cephalopoda, geographic range, southeastern Paciﬁc, species richness

Introduction them oceanic and of wide geographical distribution along the south Pacific, often exhibiting associations Present cephalopods are far from their Paleozoic

Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 with particular water masses (Rocha 1997). The splendor (Kro¨ger 2005), but they continue to be a diversity of cephalopods along the coast would very diverse and abundant group inhabiting all follow the classic pattern of increase towards lower marine environments of the world, from surface latitudes (Valdovinos 1999), in apparent relation- waters to more than 5000 m depth (Roper et al. ship with latitudinal gradients of salinity and 1984; Jereb & Roper 2005). Although some cepha- temperature, similar to the observed in other lopods are stenothermic, most species are consid- molluscs such as prosobranch gastropods (Roy ered stenohaline and eurithermic, and thus salinity et al. 1998; Rex et al. 2005), but contrasting with would be a main determinant of their geographical the inverse patterns shown by bivalvian and placo- distribution (Boyle & Rodhouse 2005; Jereb & phoran molluscs (Valdovinos 1999; Valdovinos et Roper 2005). al. 2003). The increasing diversity of prosobranch More than 90 species of Cephalopoda have been gastropods towards the tropics has been associated recorded in Chilean waters (18Á568 S), most of with variations in productivity, related in turn with

*Correspondence: Christian M. Ibań˜ez, Instituto de Ecologıá y Biodiversidad, Departamento de Ciencias Ecolo´gicas, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, N˜ unõa, Santiago, Chile. E-mail: [email protected] Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark

(Accepted 16 September 2008; Printed 23 June 2009) ISSN 1745-1000 print/ISSN 1745-1019 online # 2009 Taylor & Francis DOI: 10.1080/17451000802534873 Biogeography of cephalopods 375

the input of solar radiation and sea surface tem- the continental coast of Chile correspond to non- perature (Roy et al. 1998; Rex et al. 2005). endemic, widely distributed species. Endemic ce- However, the contrasting trends among different phalopods have been reported only on Eastern mollusc groups suggest that the above hypothesis Island and the Juan Fernańdez Archipelago (Voss should not be readily extrapolated to cephalopods, 1979; Vega et al. 2007), even though there may be especially due to the scarcity of basic information more endemic taxa which are not yet discovered and/ on their biology and ecology (Rocha 1997; Rocha & or published so far. In this context, we hypothesize Vega 2003). that the diverse sources of variation found along the Even though cephalopods have not been subject to coast are strong enough as to induce a latitudinal previous biogeographical analyses, their richness and differentiation of cephalopod distribution, as ob- distribution patterns should likely be sensitive to the served in some crustacean groups including widely high physical, chemical and geomorphological het- distributed taxa (e.g. peracarids and pelagic barna- erogeneity of the Chilean coast. Among the most cles; Thiel 2000; Hinojosa et al. 2006). Thus, this important factors affecting the geographical distri- work presents an evaluation of the latitudinal pat- bution of the Chilean marine biota (e.g. see reviews terns of diversity and distribution of cephalopod by Brattstro¨m & Johanssen 1983; Santelices 1991; species in Chile, which is also the first assessment in Rocha 1997; Fernańdez et al. 2000; Camus 2001; this coast for a group formed by a majority of non- Thiel et al. 2007), we highlight: (a) the widespread endemic components. influence of the cold Humboldt current system; (b) geographical variations of the frequency and inten- Materials and methods sity of upwelling, introducing spatial heterogeneity in local productivity and regimes of sea surface The information analysed in this paper was obtained temperature; (c) a comparatively greater influence from a review of the available literature (see Table I of physical interannual fluctuations (e.g. El Ninõ/La legend) on geographical distribution of cephalopod Ninã events) in the north-central region; (d) a species associated to the continental coast of Chile geomorphologic discontinuance due to the complete (latitudinal range: 18Á568 S), excluding those from fragmentation of the coast from 418 30’S south- oceanic islands. Thus, we first compiled a prelimin- wards, where the high input of freshwater into ary list of species and their distributions incorporat- coastal water masses promotes estuarine conditions; ing proper nomenclatural corrections when and (e) an extended oxygen minimum zone showing required. This list was then corrected and updated interannual and latitudinal variations in vertical by: (a) excluding misidentified species and uncertain extent and intensity, which attenuates from 418 S records lacking confirmation (e.g. species reported southwards. On mesoscales (tens to hundreds of either only once or from a single locality); and (b) kilometres), the above factors cause different taxa to including some new records and new species based show differential attenuation rates and latitudinal on information obtained both from field samples and limits depending on their tolerance, dispersal ability, ongoing research (Ibań˜ez et al. 2006; Cardoso, and susceptibility to external forcings. On geogra- personal communication; Ibań˜ez, unpublished phical scales (thousands of kilometres), however, data). We note that cephalopods have been less Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 major discontinuances arise from the confluence of studied or sampled than other Chilean marine latitudinal breaks of different taxa (Brattstro¨m& groups, and therefore some bias affecting our Johanssen 1983; Lancellotti & Va´squez 1999, 2000; distribution records may be inevitable. None the Fernańdez et al. 2000; Meneses & Santelices 2000; less, recent works (e.g. Rocha 1997) and informa- Santelices & Meneses 2000; Camus 2001; tion derived from an increasing number of fishery Thiel et al. 2007). studies over the whole coast (e.g. Castillo et al. Overall, three main biogeographical units can be 2007; Ibań˜ez & Cubillos 2007) have contributed to recognized along the coast: a warm-temperate area reinforce or improve the available knowledge on the in northern Chile (188 Sto30Á328 S; southern distribution of cephalopod species. Thus, although part of the Peruvian Province), a cold-temperate biases related to sampling effort may exist, they may area in austral Chile (42Á568 S; Pacific sector of be similar or even smaller than those affecting the the Magellanic Province), and a transitional area biogeographical knowledge of littoral species (e.g. between both provinces. This classification accounts see Camus 2001; Thiel et al. 2007), which are still for the distribution of many mollusc and non- largely undersampled in those areas little accessible mollusc groups, most of them with high endemism or distant from marine research centres or institu- levels. However, while several cephalopod species tions. and genera were originally described from Chilean On this basis, we generated the database employed waters, it should be noted that all valid records off in subsequent analyses, consisting of a binary matrix 376 C. M. Ibań˜ez et al.

recording the presenceÁabsence of cephalopod spe- (12.8%) distributed over the whole coast, and 1 cies every two degrees of latitude along the Chilean (1.2%) over 90% of the coast (56Á228 S). Oceanic coast (Table I), from which we obtained the number cephalopods were the most important group with 71 of species present at each latitudinal segment. Table I (82.6%) species, contrasting with coastal cephalo- also includes two types of complementary pods represented by only 15 (17.4%) species. All information: the first being a categorization of cepha- species had wide distributions independently of their lopods into coastal or oceanic species (irrespective of observed ranges in Chile: 20 (23.3%) in the Pacific their benthic or pelagic habits), which was coherent Ocean, 21 (24.4%) in the subantarctic areas (South with the classification of coastal and oceanic zones Pacific, South Atlantic and Antarctic Oceans), 9 proposed by Rocha (1997). Coastal species were (10.5%) in the Indo-Pacific Ocean and 36 (41.9%) defined as those inhabiting littoral or neritic zones in different areas worldwide (Table I). Figure 1 associated to the continental shelf, which is extremely shows the latitudinal range and position of the 86 reduced (B10 km width in some points) and narrower coastal and oceanic species along the Chilean coast, than in the northern hemisphere (Valdovinos et al. and Figure 2 shows the frequency distribution of the 2003; Cione et al. 2007), causing these species to have number of species across range size (km) classes. On a narrow longitudinal range. By contrast, oceanic the one hand, 87.2% of the species (75) exhibited at species were defined as those occurring off the least one end point of distribution within the Chilean continental shelf, the majority of which can be found coast (see Figure 1): (a) 43.0% (37: 34 oceanic, 3 between the shelf margin and 808 W (e.g. as evidenced coastal) were northern species reaching a southern in the diet of the swordfish Xiphias gladius Linnaeus, end point as they extend from warm-temperate 1758, captured between 748 and 808 W; Ibań˜ez et al. areas; (b) 27.9% (24: 17 oceanic, 7 coastal) were 2004; Castillo et al. 2007). In fact, more than 25% of southern species reaching a northern end point as oceanic species do not extend into the Pacific beyond they extend from cold-temperate areas; and (c) 808 W, although a similar proportion can extend up to 16.3% (14: 10 oceanic, 4 coastal) were species 170Á1808 W. Given that coastal and oceanic species with shorter, intra-Chilean latitudinal ranges, show- both occur in extra Chilean areas, Table I includes an ing their south and north limits mostly in north- additional descriptor aiming to reflect the extent and central or south-central positions. On the other predominant region of distribution of each species, hand, range sizes exhibited a nearly normal distribu- considering four general categories (Pacific, IndoPa- tion with most species showing intermediate ranges cific, subantarctic, worldwide). (Figure 2), with the exception of those species From the binary matrix of species by latitude (28 occurring along the whole coast. units), we generated two additional matrices separ- Overall, the number of cephalopod species (Fig- ating coastal from oceanic species. For each of the ure 3) showed a significant decreasing trend toward three matrices, we calculated a similarity matrix higher latitudes (Spearman’s rhoÁ0.721, n20, (using Jaccard’s index) to obtain a distribution p0.0003). However, such a trend was partly dendrogram by means of hierarchical cluster analysis epiphenomenic, and Figure 2 shows that it may be using the UPGM algorithm (PAST; Hammer et al. decomposed into three different subpatterns. From north to south, the number of species between 188 Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 2001). We then resampled the original binary matrix performing 1000 stochastic reassignments to gener- and 308 S exhibited a monotonic increase from 48 to 55, with an average number of 51.9 2.4 (sd) ate a distribution of similarity pseudovalues, calcu- 9 species, where the dominant component corre- lating the 95th percentile as the criterion to identify sponds to species of warm-temperate distribution significant clusters in the original similarity matrix (Figure 1). The increasing trend was due to the (Jaksic & Medel 1990). We followed a similar boot- southward incorporation of species of temperate and strap procedure to obtain the percentage of repli- cold-temperate distributions. From 308 to 328 S, the cates (1000 iterations) supporting each node of the number of species dropped to 45 due to the absence dendrogram (only values ]90% are shown). In of a number of warm-temperate components, and addition, we performed comparisons of selected gradually increased to a maximum of 57 at 428 S due dendrogram groups by means of ANOSIM (Clarke to the incorporation of both short-range temperate 1993; Hammer et al. 2001). components and cold-temperate components (Fig- ure 1), with an average number for this area of Results 48.894.5 (sd) species. Between 428 and 448 S, the confluence of many southern and northern end- Diversity points of distribution marks an important faunal We recorded a total of 86 non-endemic cephalopod replacement (Figure 1), causing a strong decrease species in Chile (Table I, Figure 1), 11 of them from 57 to 35 species. The area from 448 to 568 was Table I. List of studied species and their geographical distribution in the Chilean coast. The information on distribution was obtained from Thore (1959), Nesis (1972, 1987, 1993), Retamal & Orellana (1977), Roper et al. (1984), Okutani & Clarke (1985), Andrade (1987), Voss (1988), Rocha et al. (1991), Alexeyev (1993, 1994a,b), Rocha (1997), Dunning (1998), Kubodera et al. (1998), Voss et al. (1998), Wormuth (1998), Valdovinos (1999), Villarroel et al. (2001), Ibań˜ez et al. (2004), Castillo et al. (2007), and Ibań˜ez (unpublished data). Records marked by asterisks correspond to taxa currently placed into a different genus (*) or in the process of being described as new species (**).

Latitudinal distribution off Chile

Species Habitat Distribution 188 208 228 248 268 288 308 328 348 368 388 408 428 448 468 488 508 528 548 568

Stoloteuthis sp. Verrill, 1881** Coastal Pacific XXXXXXX Rossia glaucopis Loven, 1845 Coastal Worldwide XXXXXXXX Rossia mastigophora Berry, 1911 Coastal IndoPacific X X X Semirossia patagonica (Smith, 1881) Coastal Pacific XXXXXXXXXXX Neorossia caroli (Joubin, 1902) Coastal Worldwide X X Heteroteuthis sp. Gray, 1849 Oceanic Pacific XXXXXXX Iridoteuthis sp. Naef, 1912 Oceanic Pacific XXXXXXX Loligo gahi Orbigny, 1835 Coastal Subantarctic XXXXXXXXXXXXXXXXXXXX Lycoteuthis diadema (Chun, 1900) Oceanic Worldwide XXXXXXXXXXXXX Enoploteuthis sp. Orbigny, 1844 Oceanic Pacific XXXXXXXXX Enoploteuthis semilineata Alexeyev, 1994 Oceanic Pacific XXXXX Abraliopsis affinis (Pfeffer, 1912) Oceanic Pacific X X X Abraliopsis gilchristi (Robson, 1924) Oceanic Worldwide XXXXXXXXXXX Ancistrocheirus alessandrinii (Ve´rany, 1851) Oceanic Pacific XXXXX Pterygoteuthis gemmata Chun, 1910 Oceanic IndoPacific XXXXXXXXXXXXX Pterygoteuthis giardi hoylei (Pfeffer, 1912) Oceanic Worldwide XXXXXXXXXXXXX Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 June 16 19:01 At: M.] Christian [Ibáñez, By: Downloaded Pyroteuthis margaritifera (Ru¨ppel, 1844) Oceanic Worldwide XXXXXXXXXX Octopoteuthis deletron Young, 1972 Oceanic Pacific X X Octopoteuthis nielseni (Robson, 1948) Oceanic Pacific XXXXXXXXXXXXX Onychoteuthis banksii (Leach, 1817) Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX Moroteuthis ingens (Smith, 1881) Oceanic Subantarctic XXXXXXXX Moroteuthis knipovitchi Filippova, 1972 Oceanic Subantarctic XXXXXXXX Moroteuthis robsoni Adam, 1962 Oceanic Worldwide XXXXXXXXXXX Kondakovia longimana Filippova, 1971 Oceanic Subantarctic XXX Discoteuthis discus Young & Roper, 1969 Oceanic Worldwide XXXXXXX igorpyo cephalopods of Biogeography Gonatus antarcticus Lo¨nnberg, 1898 Oceanic Subantarctic XXXXXXXXXXXXXXXXXXXX Pholidoteuthis boschmani Adam, 1950 Oceanic Worldwide XXXXXXXX Architeuthis dux Steenstrup, 1857 Oceanic Worldwide XXXXXXXXXXXXXX Histioteuthis atlantica (Hoyle, 1885) Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX Histioteuthis corona cerasina Nesis, 1971 Oceanic Pacific XXXXXXXXXXXXX Histioteuthis dofleini (Pfeffer, 1912) Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX Histioteuthis eltaninae Voss, 1969 Oceanic Subantarctic XXXXXXX Histioteuthis hoylei (Goodrich, 1896) Oceanic Worldwide XXXXXXXXXX Histioteuthis heteropsis (Berry, 1918) Oceanic Pacific XXXXXXXXXX Neoteuthis sp. Naef, 1921 Oceanic IndoPacific XXXXXXX Nototeuthis dimegacotyle Nesis & Nikitina, Oceanic Worldwide XXXXXXXXXX 1986*

Bathyteuthis abyssicola Hoyle, 1885 Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX377 Brachioteuthis picta Chun, 1910 Oceanic Subantarctic XXXXXXXXXXXXX 378 Table I (Continued) Latitudinal distribution off Chile .M Iba M. C. Species Habitat Distribution 188 208 228 248 268 288 308 328 348 368 388 408 428 448 468 488 508 528 548 568

Brachioteuthis riisei/ (Steenstrup, 1882) Oceanic Worldwide XXXXXXXXXXXXX

Batoteuthis skolops Young & Roper, 1968 Oceanic Subantarctic XXXX´ n ˜ Todarodes filippovae Adam, 1975 Oceanic Worldwide XXXXXXXXXXXXXXXXXX al. et ez Martialia hyadesi Rochebrune & Mabille, Oceanic Subantarctic XXXXXXXXXXXXXX 1889 Nototodarus hawaiiensis (Berry, 1912) Oceanic Pacific XXXXXXX Ommastrephes bartramii (Leseur, 1821) Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX Dosidicus gigas (Orbigny, 1835) Oceanic Pacific XXXXXXXXXXXXXXX Sthenoteuthis oualaniensis (Lesson, 1830) Oceanic IndoPacific XXXXX Eucleoteuthis luminosa Sasaki, 1915 Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX Chiroteuthis veranyi (Fe´russac, 1835) Oceanic Subantarctic XXXXXXXXXXXXXXXXXXXX Planctoteuthis sp. Pfeffer, 1912* Oceanic Worldwide XXXXXXXXXXXXX Planctoteuthis danae (Joubin, 1931)* Oceanic Pacific XXXXXXXXXXXXX Mastigoteuthis agassizii (Verrill, 1881) Oceanic Worldwide XXXXXXXXXXXXXXXXXXXX Mastigoteuthis famelica Berry, 1909 Oceanic Worldwide XXXXXXXX Promachoteuthis sp. Hoyle, 1885 Oceanic Subantarctic XXXXXXXXXXXXXX Taonius sp. Steenstrup, 1861 Oceanic Pacific XXXXXXXX Cranchia scabra Leach, 1817 Oceanic Worldwide XXXXXXXXXX Liocranchia reinhardtii (Steenstrup, 1856) Oceanic Worldwide XXXXXXXXXXXXX

Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 June 16 19:01 At: M.] Christian [Ibáñez, By: Downloaded Leachia cyclura LeSueur, 1821 Oceanic Worldwide XXXXXXX Leachia dislocata Young, 1971 Oceanic IndoPacific X X Leachia pacifica (Issel, 1908) Oceanic Subantarctic XXXXXX Leachia rhynchophorus (Rochebrune, 1884) Oceanic Subantarctic XXXX Helicocranchia pfefferi Massy, 1907 Oceanic Worldwide XXXXXXXXXXXXX Galiteuthis pacifica (Robson, 1948) Oceanic IndoPacific XXXXXXX Galiteuthis suhmi (Hoyle, 1885) Oceanic Worldwide XXXXXXXXXXX Bathotauma lyromma Chun, 1906 Oceanic Worldwide XXXXXXXXXXXXX Megalocranchia abyssicola (Goodrich, 1896) Oceanic Worldwide XXXXXXXXXXXXX Mesonychoteuthis hamiltoni Robson, 1925 Oceanic Subantarctic XXXXXX Teuthowenia pellucida (Chun, 1910) Oceanic Subantarctic XXXXXXXX Vampyroteuthis infernalis Chun, 1910 Oceanic Worldwide XXXXXXXXXXXXX Cirrothauma murrayi Chun, 1911 Oceanic Worldwide XXXXXXXXX Opisthoteuthis sp. Verrill, 1883** Oceanic Pacific XXXXXX Japetella diaphana Hoyle, 1885 Oceanic Worldwide XXXXXXXXXXXXX Eledonella pygmaea Verrill, 1884 Oceanic Worldwide XXXXXXX Robsonella fontaniana (Orbigny, 1834) Coastal Subantarctic XXXXXXXXXXXXXXXXXXXX Enteroctopus megalocyathus (Gould, 1852) Coastal Subantarctic XXXXXXXX Octopus mimus Gould, 1852 Coastal Pacific XXXXXXXXX Scaeurgus patagiatus Berry, 1913* Oceanic IndoPacific XXXXXXX Pteroctopus hoylei (Berry, 1909)* Oceanic IndoPacific XXXXXXX Thaumeledone brevis (Hoyle, 1885) Coastal Subantarctic XX Graneledone sp. Joubin, 1918** Coastal Pacific XXXXXXXXXXXXX Pareledone charcoti (Joubin, 1905) Coastal Subantarctic XXXXXXXXX Biogeography of cephalopods 379 8

56 dominated by cold-temperate and subantarctic components, showing a low and nearly homogeneous 8

54 species richness, with an average of 35.090.8 (sd)

8 species and fluctuating between 34 to 36 species. 52 8

50 Latitudinal distribution

8 Cluster analysis for all cephalopod species showed 48 three major groupings (Figure 4A), separating 8 northern (18Á308 S), central (30Á428 S) and south- 46 ern (42Á568 S) areas on the Chilean coast. Due to 8

44 the wide distribution of most species, the overall

8 similarity of latitudinal ranges was very high with a

42 95th percentile of 94%, generating several mesoscale

8 significant clusters within northern and southern XXXXXXXXX XXXXXXXXX 40 areas, and none within the central area. However, 8 the three major nodes were consistent and supported 38 by bootstrap estimates between 93 and 100%, and 8

36 the three groups exhibited significant differences (ANOSIM, r 0.99, p 0.001). 8 B

34 When the original matrix was disaggregated into

8 coastal and oceanic species, we observed slightly Latitudinal distribution off Chile 32 different results. The clustering of oceanic species

8 (Figure 4B) maintained the spatial structure of the 30 whole data set, also with a 95th percentile of 8 similarity of 94%, and bootstrap estimates between 28 94 and 100% for the three nodes comprising the 8

26 northern, central and southern areas. However,

8 coastal species (Figure 4C) exhibited a lower overall

24 similarity with a 95th percentile of 85%, and much

8 lower bootstrap estimates for all dendrogram nodes 22 (all B90%) for the three nodes. 8 Thus, the detection of the two main biogeogra- XXXXXXXXX 20 phical discontinuances at 308 and 428 S appeared 8

XXXXXXXXXXXXX XXXXXXXXXXXXX XXXXXXXXXXXXX robust because of their correspondence with the two latitudinal peaks in species numbers (Figure 3), and the fact that 51.2% of the species (44) showed either a northern or southern limit of distribution at those

Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 latitudes (Figure 1): (a) 16 end points at 308 S, contributed by 11 northern, 2 southern, and 3 intra- Chilean species (18.6% of species); and (b) 28 end points at 428 S, from 17 northern, 7 southern, and 4 Coastal Pacific Oceanic IndoPacific intra-Chilean species (32.6% of species). lveda

´ Discussion Diversity ez, Sepu ˜ (Eydoux &

ń The available data indicate that cephalopod species (Robson, 1930) Coastal Subantarctic Iba showed marked biogeographical changes over the Chilean coast. The number of species was little (Joubin, 1905) Coastal Subantarctic ) Solander, 1786 Oceanic Worldwide variable in the northern zone (18 308 S) due to the Solander, 1786 Oceanic Worldwide Á massive penetration of species extending from lower latitudes. Notably, the number of cephalopod spe- Continued cies undergoes only minor changes from the equator to northern Chile (Ibań˜ez, unpublished data), sug- & Chong, 2006 Souleyet, 1852) Species Habitat Distribution 18 Table I ( Benthoctopus longibrachus Pareledone turqueti Benthoctopus magellanicus Tremoctopus violaceus gracilis Argonauta hians Argonauta nodosa gesting that they face no effective barrier over most 380 C. M. Ibań˜ez et al.

Figure 1. Latitudinal range (vertical bars) of coastal and oceanic cephalopod species off the Chilean coast. Horizontal lines mark the northern (308 S) and southern (428 S) boundaries of the transitional area between the warm- and cold-temperate biogeographic units over the coast.

of the Pacific South American coast. However, which could exceed the tolerance limits of many several northern species do not extend south of species. In addition, the austral region formed by 30Á328 S, where the subtropical oceanic conver- fjords and channels exhibits some important off- gence occurs (Farinã et al. 2006) and the number of shoreÁcoast gradients in salinity and sea surface species drops from 55 to 45. Thus, it is likely that temperature (e.g. Da´vila et al. 2002; Figueroa external forcings may prevent the dispersal of these 2002; Silva & Guzmań 2006), which make coastal cephalopods further south, such as the strong physical conditions very restrictive and may prevent changes in eddy activity and wind stress occurring oceanic species to reach nearshore habitats. at 308 S (Hormaza´bal et al. 2004), and the con- Overall, the number of cephalopod species de- trasting productivity between coastal and offshore creases on average from northern to southern Chile, zones at the same latitude (see Thiel et al. 2007). A a similar trend to that observed for other Chilean second and most important change occurs at 428 S, taxa (e.g. Lancellotti & Va´squez 2000; Ojeda et al. coincident with the West Wind Drift oceanic con- 2000; Astorga et al. 2003), and also for taxa from the vergence (Farinã et al. 2006). At this latitude, most northern hemisphere (e.g. Roy et al. 1998; Rex et al. northern species end their distribution, and the 2000). However, we remark that the decrease in number of species exhibits a sharp decrease being diversity is far from monotonic and occurs at reduced by nearly 50%. The whole area between 428 discrete steps, mainly as a by-product of the dis- and 568 S exhibits a similarly low diversity, being tributional breaks at 308 and 428 S, where the

Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 dominated by cold-water and subantarctic species. overlap between southern and northern cephalopods The main factors associated with this break in causes species number to peak. Thus, we should richness could be the decrease in salinity and refer this trend as a between-region decrease in the temperature south of 428 S (see Camus 2001), mean number of species (northcentralsouthern

Figure 2. Frequency distribution of the number of cephalopod species by range size (km) classes. Biogeography of cephalopods 381

Figure 3. Number of cephalopod species recorded every two degrees of latitude over the Chilean coast.

Chile). Such abrupt transitions suggest that the distribution of cephalopods follows the traditional diversity and geographical extent of non-endemic differentiation into three biogeographical units: a cephalopods in Chile are controlled by the presence northern area (18Á308 S) comprising the southern or absence of major physical forcings. In turn, this part of the warm-temperate Peruvian province, a may be the main noticeable difference between southern area (42Á568 S) comprising the cold- cephalopods and taxa with endemic components, temperate Magellanic province, and an intermediate as these latter tend to show slightly clearer gradients transitional area (30Á428 S) characterized by the of diversity along the coast (see reviews by Lancel- overlapping distribution of warm- and cold-water lotti & Va´squez 2000; Camus 2001; Thiel et al. species. Outside the Chilean coast, cephalopod 2007). species occurring at the northern area have char- acteristic subtropical and temperate distributions Distribution (e.g. Roper et al. 1984), while all species occurring at the southern area have also a subantarctic Cephalopods as a whole show well-defined biogeo- distribution (e.g. Okutani & Clarke 1985; Boyle & graphic groupings, with two main species replace- Rodhouse 2005). ments at 308 and 428 S differentiating northern, As mentioned above, the fact that such euritermic, central and southern areas. As expected, however, non-endemic species show well-defined distribution these three groups are not statistically significant at endpoints within the Chilean coast suggest that p0.05 because nearly 30% of species are distrib- external forcings may be more important than uted either in the whole coast (18Á568 S) or in the previously thought, especially considering the high north-central zone (18Á428 S), leading to a high level dispersal potential of many species through their of similarity between any pair of latitudes. None- Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 planctonic paralarvae (Rocha et al. 1999; Gonza´lez theless, the three areas are defined by nodes at least at 70% of similarity and well supported by bootstrap et al. 2005; Jereb & Roper 2005). The similar estimates, what we consider to be a consistent latitudinal breaks shown by a number of endemic clustering for a coastal range of 4500 km where taxa are often interpreted as a response to physical 57% of species have distribution ranges greater than gradients dependent on their tolerance ranges, 2000 km. Oceanic cephalopods represent ca. 83% of particularly to water temperature. For instance, species, and therefore their clustering pattern is strong interannual thermal fluctuations such as El virtually the same as described above. The small Ninõ events are known to affect cephalopod species, group of coastal cephalopods shows a statistically leading to abundance increases in coastal benthic weak patterning, but nonetheless most of them tend octopuses (Castilla & Camus 1992) or abundance to have smaller distribution ranges which also exhibit decreases and distribution variations in neritic and a clear latitudinal segregation into northern, central oceanic squids (Anderson & Rodhouse 2001; Ville- and southern areas. gas 2001; Rocha & Vega 2003). Similar variations Our results show that the biogeographical patterns can be observed in many algal and invertebrate taxa of non-endemic cephalopod species in Chile have no of diverse phyletic origin (e.g. Va´squez et al. 2006; particular differences with those already described Thiel et al. 2007; Camus 2008). However, several of for most Chilean taxa (summarized by Fernańdez et these taxa are also known to have upper tolerance al. 2000; Camus 2001; Thiel et al. 2007). The limits exceeding the highest temperatures recorded 382 C. M. Ibań˜ez et al.

Figure 4. Hierarchical clustering of the presenceÁabsence of cephalopod species in 28 latitudinal bands in the Chilean coast. A, all species; B, oceanic species; C, coastal species. The vertical line inside each dendrogram marks the 95th percentile of similarity obtained from stochastic reassignments of the original binary matrix. Nodes include values of bootstrap estimates (only values ]90% are shown).

during El Ninõ events (Wolff 1987; Urban 1994), Ibań˜ez was supported by a CONICYT doctoral Downloaded By: [Ibáñez, Christian M.] At: 19:01 16 June 2009 and thus interannual variations cannot easily explain fellowship. their biogeographical patterns. The same may occur with latitudinal variations of sea surface temperature, which cannot explain the variations of mollusc References diversity along the coast, while continental shelf area appears as a key determinant (e.g. Valdovinos et al. Alexeyev DO. 1993. New data on the squid fauna of the Southern Pacific. Southern Ocean Cephalopods Symposium, Cambridge 2003). Thus, we suggest that the marked distribu- 4Á10 July 1993. 18 pages. tion breaks of cephalopods may reflect the action of Alexeyev DO. 1994a. Enoploteuthis (Paraenoploteuthis) semilineata, external forcings or factors other than temperature, a new species of squid (Cephalopoda, Oegopsida, Enoplo- which should also be important determinants for teuthidae) from the Southern Pacific. Ruthenica 4(2):167Á71. endemic species acting as constraints or barriers to Alexeyev DO. 1994b. New data on the distribution and biology of squid from the Southern Pacific. Ruthenica 4(2):151 66. dispersal. Á Anderson CIH, Rodhouse PG. 2001. Life cycles, oceanography and variability: Ommastrephid squid in variable oceanographic environments. Fisheries Research 54:133Á43. Acknowledgements Andrade H. 1987. Distribucioń batime´trica y geogra´fica de macroinvertebrados del talud continental de Chile central. We thank valuable comments and suggestions by Ciencia y Tecnologıá del Mar 11:61Á94. Hugo I. Moyano, Pilar Sańchez, Angel Guerra and Astorga A, Fernańdez M, Boschi EE, Lagos N. 2003. Two oceans, Cristiań E. Hernańdez on an earlier draft. C. M. two taxa and one mode of development: Latitudinal diversity Biogeography of cephalopods 383

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